The fMRI correlates of visuo-spatial abilities: sex differences and gender dysphoria

Springer Science and Business Media LLC - Tập 16 - Trang 955-964 - 2022
Gioele Gavazzi1, Alessandra Daphne Fisher2, Stefano Orsolini3, Andrea Bianchi4, Alessia Romani2, Fiorenza Giganti5, Fabio Giovannelli5, Jiska Ristori2, Francesca Mazzoli2, Mario Maggi2, Maria Pia Viggiano5, Mario Mascalchi2
1IRCCS SDN, Naples, Italy
2“Mario Serio” Department of Experimental and Clinical Biomedical Sciences, University of Florence, Florence, Italy
3Department of Electrical, Electronic and Information Engineering “Guglielmo Marconi,” University of Bologna, Cesena, Italy
4Neuroradiology Unit, “Careggi” University Hospital, Florence, Italy
5Department of Neuroscience, Psychology, Drug Research, Child Health, University of Florence, Florence, Italy

Tóm tắt

The contribution of brain regions to visuospatial abilities according to sex differences and gender identity is inconsistently described. One potential explaining factor may be the different tasks employed requiring a variable load of working memory and other cognitive resources. Here we asked to 20 cis and 20 transgender participants to undergo functional Magnetic Resonance Imaging during performance of a judgement line of orientation test that was adapted to explore the basic visuospatial processing while minimizing the working memory load. We show that V1 activation may be viewed as a brain area with enhanced activation in males, regardless of participants’ gender identity. On its turn, gender identity exclusively influences the visuospatial processing of extrastriate visual areas (V5) in women with gender dysphoria. They showed enhanced V5 activation and an increased functional connectivity between V5 and V1. Overall our neuroimaging results suggest that the basic visuospatial abilities are associated with different activations pattern of cortical visual areas depending on the sex assigned at birth and gender identity.

Tài liệu tham khảo

Adesnik, H., Bruns, W., Taniguchi, H., Huang, Z. J., & Scanziani, M. (2012). A neural circuit for spatial summation in visual cortex. Nature, 490(7419), 226–231. https://doi.org/10.1038/nature11526 Bao, A.-M., & Swaab, D. F. (2011). Sexual differentiation of the human brain: Relation to gender identity, sexual orientation and neuropsychiatric disorders. Frontiers in Neuroendocrinology, 32(2), 214–226. https://doi.org/10.1016/j.yfrne.2011.02.007 Beatty, W. W. (2002). Sex difference in geographical knowledge: Driving experience is not essential. Journal of the International Neuropsychological Society: JINS, 8(6), 804–810. https://doi.org/10.1017/s1355617702860088 Benton, A., Hannay, H. J., & Varney, N. R. (1975). Visual perception of line direction in patients with unilateral brain disease. Neurology, 25(10), 907–910. https://doi.org/10.1212/wnl.25.10.907 Burke, S. M., Kreukels, B. P. C., Cohen-Kettenis, P. T., Veltman, D. J., Klink, D. T., & Bakker, J. (2016). Male-typical visuospatial functioning in gynephilic girls with gender dysphoria—Organizational and activational effects of testosterone. Journal of Psychiatry & Neuroscience: JPN, 41(6), 395–404. https://doi.org/10.1503/jpn.150147 Campana, G., Cowey, A., & Walsh, V. (2005). Visual area V5/MT remembers «What» but Not «Where». Cerebral Cortex, 16(12), 1766–1770. https://doi.org/10.1093/cercor/bhj111 Clements, A. M., Rimrodt, S. L., Abel, J. R., Blankner, J. G., Mostofsky, S. H., Pekar, J. J., Denckla, M. B., & Cutting, L. E. (2006). Sex differences in cerebral laterality of language and visuospatial processing. Brain and Language, 98(2), 150–158. https://doi.org/10.1016/j.bandl.2006.04.007 Clements-Stephens, A. M., Rimrodt, S. L., & Cutting, L. E. (2009). Developmental sex differences in basic visuospatial processing: Differences in strategy use? Neuroscience Letters, 449(3), 155–160. https://doi.org/10.1016/j.neulet.2008.10.094 Cohen-Bendahan, C. C. C., van de Beek, C., & Berenbaum, S. A. (2005). Prenatal sex hormone effects on child and adult sex-typed behavior: Methods and findings. Neuroscience and Biobehavioral Reviews, 29(2), 353–384. https://doi.org/10.1016/j.neubiorev.2004.11.004 Desikan, R. S., Ségonne, F., Fischl, B., Quinn, B. T., Dickerson, B. C., Blacker, D., Buckner, R. L., Dale, A. M., Maguire, R. P., Hyman, B. T., Albert, M. S., & Killiany, R. J. (2006). An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. NeuroImage, 31(3), 968–980. https://doi.org/10.1016/j.neuroimage.2006.01.021 Diedrichsen, J., Maderwald, S., Küper, M., Thürling, M., Rabe, K., Gizewski, E. R., Ladd, M. E., & Timmann, D. (2011). Imaging the deep cerebellar nuclei: A probabilistic atlas and normalization procedure. NeuroImage, 54(3), 1786–1794. https://doi.org/10.1016/j.neuroimage.2010.10.035 Doyle, R. A., Voyer, D., & Cherney, I. D. (2012). The relation between childhood spatial activities and spatial abilities in adulthood. Journal of Applied Developmental Psychology, 33(2), 112–120. https://doi.org/10.1016/j.appdev.2012.01.002 Eickhoff, S. B., Paus, T., Caspers, S., Grosbras, M.-H., Evans, A. C., Zilles, K., & Amunts, K. (2007). Assignment of functional activations to probabilistic cytoarchitectonic areas revisited. NeuroImage, 36(3), 511–521. https://doi.org/10.1016/j.neuroimage.2007.03.060 Eliot, L., Ahmed, A., Khan, H., & Patel, J. (2021). Dump the “dimorphism”: Comprehensive synthesis of human brain studies reveals few male-female differences beyond size. Neuroscience & Biobehavioral Reviews, 125, 667–697. https://doi.org/10.1016/j.neubiorev.2021.02.026 Elkhetali, A. S., Fleming, L. L., Vaden, R. J., Nenert, R., Mendle, J. E., & Visscher, K. M. (2019). Background connectivity between frontal and sensory cortex depends on task state, independent of stimulus modality. NeuroImage, 184, 790–800. https://doi.org/10.1016/j.neuroimage.2018.09.040 Fair, D. A., Schlaggar, B. L., Cohen, A. L., Miezin, F. M., Dosenbach, N. U. F., Wenger, K. K., Fox, M. D., Snyder, A. Z., Raichle, M. E., & Petersen, S. E. (2007). A method for using blocked and event-related fMRI data to study “resting state” functional connectivity. NeuroImage, 35(1), 396–405. https://doi.org/10.1016/j.neuroimage.2006.11.051 Fisher, A. D., Ristori, J., Castellini, G., Cocchetti, C., Cassioli, E., Orsolini, S., et al. (2020). Neural correlates of gender face perception in transgender people. Journal of Clinical Medicine, 9(6), 1731. https://doi.org/10.3390/jcm9061731 Franzen, M. D. (2000). Reliability and validity in neuropsychological assessment (2nd ed.). Kluwer Academic/Plenum Publishers. Gavazzi, G., Orsolini, S., Rossi, A., Bianchi, A., Bartolini, E., Nicolai, E., Soricelli, A., Aiello, M., Diciotti, S., Viggiano, M. P., & Mascalchi, M. (2017). Alexithymic trait is associated with right IFG and pre-SMA activation in non-emotional response inhibition in healthy subjects. Neuroscience Letters, 658, 150–154. https://doi.org/10.1016/j.neulet.2017.08.031 Gavazzi, G., Rossi, A., Orsolini, S., Diciotti, S., Giovannelli, F., Salvadori, E., Pantoni, L., Mascalchi, M., & Viggiano, M. P. (2019). Impulsivity trait and proactive cognitive control: An fMRI study. The European Journal of Neuroscience, 49(9), 1171–1179. https://doi.org/10.1111/ejn.14301 Gold, A. U., Pendergast, P. M., Ormand, C. J., Budd, D. A., Stempien, J. A., Mueller, K. J., & Kravitz, K. A. (2018). Spatial skills in undergraduate students—Influence of gender, motivation, academic training, and childhood play. Geosphere, 14(2), 668–683. https://doi.org/10.1130/GES01494.1 Goldstein, D., Haldane, D., & Mitchell, C. (1990). Sex differences in visual-spatial ability: The role of performance factors. Memory & Cognition, 18(5), 546–550. https://doi.org/10.3758/BF03198487 Hill, A. C., Laird, A. R., & Robinson, J. L. (2014). Gender differences in working memory networks: A BrainMap meta-analysis. Biological Psychology, 102, 18–29. https://doi.org/10.1016/j.biopsycho.2014.06.008 Hugdahl, K., Thomsen, T., & Ersland, L. (2006). Sex differences in visuo-spatial processing: An fMRI study of mental rotation. Neuropsychologia, 44(9), 1575–1583. https://doi.org/10.1016/j.neuropsychologia.2006.01.026 Iacaruso, M. F., Gasler, I. T., & Hofer, S. B. (2017). Synaptic organization of visual space in primary visual cortex. Nature, 547(7664), 449–452. https://doi.org/10.1038/nature23019 John, & Raven, J. (2003). Raven progressive matrices. In R. S. McCallum (A c. Di), Handbook of nonverbal assessment (pagg. 223–237). Springer US. https://doi.org/10.1007/978-1-4615-0153-4_11 Johnson, A. M. (1990). The speed of mental rotation as a function of problem-solving strategies. Perceptual and Motor Skills, 71(3 Pt 1), 803–806. https://doi.org/10.2466/pms.1990.71.3.803 Johnson, E. S., & Meade, A. C. (1987). Developmental patterns of spatial ability: An early sex difference. Child Development, 58(3), 725–740. https://doi.org/10.1111/j.1467-8624.1987.tb01413.x Karádi, K., Csathó, A., Kovács, B., & Kosztolányi, P. (2003). Subgroup analysis of sex difference on the Vandenberg-Kuse mental rotation test. Perceptual and Motor Skills, 96(1), 197–200. https://doi.org/10.2466/pms.2003.96.1.197 Kesler, S. R. (2004). Functional neuroanatomy of spatial orientation processing in turner syndrome. Cerebral Cortex, 14(2), 174–180. https://doi.org/10.1093/cercor/bhg116 Kimura, D. (1996). Sex, sexual orientation and sex hormones influence human cognitive function. Current Opinion in Neurobiology, 6(2), 259–263. https://doi.org/10.1016/s0959-4388(96)80081-x Koenigs, M., Barbey, A. K., Postle, B. R., & Grafman, J. (2009). Superior parietal cortex is critical for the manipulation of information in working memory. Journal of Neuroscience, 29(47), 14980–14986. https://doi.org/10.1523/JNEUROSCI.3706-09.2009 Kreukels, B. P. C., & Guillamon, A. (2016). Neuroimaging studies in people with gender incongruence. International Review of Psychiatry (abingdon, England), 28(1), 120–128. https://doi.org/10.3109/09540261.2015.1113163 Linn, M. C., & Petersen, A. C. (1985). Emergence and characterization of sex differences in spatial ability: A meta-analysis. Child Development, 56(6), 1479–1498. Lippa, R. A., Collaer, M. L., & Peters, M. (2010). Sex differences in mental rotation and line angle judgments are positively associated with gender equality and economic development across 53 nations. Archives of Sexual Behavior, 39(4), 990–997. https://doi.org/10.1007/s10508-008-9460-8 Mueller, S. C., Guillamon, A., Zubiaurre-Elorza, L., Junque, C., Gomez-Gil, E., Uribe, C., et al. (2021). The neuroanatomy of transgender identity: Mega-analytic findings from the ENIGMA transgender persons working group. The Journal of Sexual Medicine, 18(6), 1122–1129. https://doi.org/10.1016/j.jsxm.2021.03.079 Park, J., Papoutsi, A., Ash, R. T., Marin, M. A., Poirazi, P., & Smirnakis, S. M. (2019). Contribution of apical and basal dendrites to orientation encoding in mouse V1 L2/3 pyramidal neurons. Nature Communications, 10(1), 5372. https://doi.org/10.1038/s41467-019-13029-0 Peters, M. (2005). Sex differences and the factor of time in solving Vandenberg and Kuse mental rotation problems. Brain and Cognition, 57(2), 176–184. https://doi.org/10.1016/j.bandc.2004.08.052 Podzebenko, K., Egan, G. F., & Watson, J. D. G. (2002). Widespread dorsal stream activation during a parametric mental rotation task, revealed with functional magnetic resonance imaging. NeuroImage, 15(3), 547–558. https://doi.org/10.1006/nimg.2001.0999 Reich, S. M., Black, R. W., & Foliaki, T. (2018). Constructing difference: Lego® set narratives promote stereotypic gender roles and play. Sex Roles, 79(5–6), 285–298. https://doi.org/10.1007/s11199-017-0868-2 Ristori, J., Cocchetti, C., Romani, A., Mazzoli, F., Vignozzi, L., Maggi, M., & Fisher, A. D. (2020). Brain sex differences related to gender identity development: Genes or hormones? International Journal of Molecular Sciences, 21(6), 2123. https://doi.org/10.3390/ijms21062123 Ritchie, S. J., Cox, S. R., Shen, X., Lombardo, M. V., Reus, L. M., Alloza, C., Harris, M. A., Alderson, H. L., Hunter, S., Neilson, E., Liewald, D. C. M., Auyeung, B., Whalley, H. C., Lawrie, S. M., Gale, C. R., Bastin, M. E., McIntosh, A. M., & Deary, I. J. (2018). Sex differences in the adult human brain: Evidence from 5216 UK Biobank participants. Cerebral Cortex, 28(8), 2959–2975. https://doi.org/10.1093/cercor/bhy109 Saykin, A. J., Gur, R. C., Gur, R. E., Shtasel, D. L., Flannery, K. A., Mozley, L. H., Malamut, B. L., Watson, B., & Mozley, P. D. (1995). Normative neuropsychological test performance: Effects of age, education, gender and ethnicity. Applied Neuropsychology, 2(2), 79–88. https://doi.org/10.1207/s15324826an0202_5 Smith, S., & Nichols, T. (2009). Threshold-free cluster enhancement: Addressing problems of smoothing, threshold dependence and localisation in cluster inference. NeuroImage, 44(1), 83–98. https://doi.org/10.1016/j.neuroimage.2008.03.061 Sun, W., Tan, Z., Mensh, B. D., & Ji, N. (2016). Thalamus provides layer 4 of primary visual cortex with orientation- and direction-tuned inputs. Nature Neuroscience, 19(2), 308–315. https://doi.org/10.1038/nn.4196 Unterrainer, J., Wranek, U., Staffen, W., Gruber, T., & Ladurner, G. (2000). Lateralized cognitive visuospatial processing: Is it primarily gender-related or due to quality of performance? A HMPAO-SPECT study. Neuropsychobiology, 41(2), 95–101. https://doi.org/10.1159/000026639 Vandenberg, S. G., & Kuse, A. R. (1978). Mental rotations, a group test of three-dimensional spatial visualization. Perceptual and Motor Skills, 47(2), 599–604. https://doi.org/10.2466/pms.1978.47.2.599 Voyer, D., Voyer, S., & Bryden, M. P. (1995). Magnitude of sex differences in spatial abilities: A meta-analysis and consideration of critical variables. Psychological Bulletin, 117(2), 250–270. https://doi.org/10.1037/0033-2909.117.2.250